Parallel processing in the honeybee olfactory pathway: structure, function, and evolution

Abstract

Animals face highly complex and dynamic olfactory stimuli in their natural environments, which require fast and reliable olfactory processing. Parallel processing is a common principle of sensory systems supporting this task, for example in visual and auditory systems, but its role in olfaction remained unclear. Studies in the honeybee focused on a dual olfactory pathway. Two sets of projection neurons connect glomeruli in two antennal-lobe hemilobes via lateral and medial tracts in opposite sequence with the mushroom bodies and lateral horn. Comparative studies suggest that this dual-tract circuit represents a unique adaptation in Hymenoptera. Imaging studies indicate that glomeruli in both hemilobes receive redundant sensory input. Recent simultaneous multi-unit recordings from projection neurons of both tracts revealed widely overlapping response profiles strongly indicating parallel olfactory processing. Whereas lateral-tract neurons respond fast with broad (generalistic) profiles, medial-tract neurons are odorant specific and respond slower. In analogy to “what-” and “where” subsystems in visual pathways, this suggests two parallel olfactory subsystems providing “what-” (quality) and “when” (temporal) information. Temporal response properties may support across-tract coincidence coding in higher centers. Parallel olfactory processing likely enhances perception of complex odorant mixtures to decode the diverse and dynamic olfactory world of a social insect.Electronic supplementary materialThe online version of this article (doi:10.1007/s00359-013-0821-y) contains supplementary material, which is available to authorized users.

Simultaneous Long-term Recordings at Two Neuronal Processing Stages in Behaving Honeybees

“…However, the temporal resolution of the imaging process itself is rather limited. Optical acquisition systems usually use CCD-imaging with a temporal resolution of [5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20] , although 2-PhotonImaging might be able to acquire faster sequences 68 . However, increasing sampling rate always goes along with a loss in spatial resolution.…”

“…Both ALTs (l-and m-ALT) combine either 410 (l-ALT) or 510 (m-ALT) uniglomerular projection neurons (PN), respectively 15,16,19 . PNs of both tracts have recently been shown to code odors in parallel 2 (for review see 17,20 ), and both tracts synaptically form divergent connections with Kenyon Cells (KC), the mushroom body (MB) principal neurons. Each MB contains about 172,000 KCs [21][22][23] .…”

Parallel pathways convey olfactory information with opposite polarities in Drosophila

“…For instance, by combining electrical/optical recordings and modeling, researchers found that in Hymenopterans, two separate pathways formed by uniglomerular PNs that innervating nonoverlapping glomeruli convey information with similar profiles, although the odor selectivity is higher in the medial pathway and the response delay is shorter in the lateral pathway (7)(8)(9)(10)(11). Also, recent progress in Lepidopterans suggest that two parallel olfactory pathways are responsible for the innate and learned behaviors, respectively (12).…”

“…After AL local processing, olfactory information is relayed to higher brain regions via different groups of projection neurons (PNs) (4)(5)(6). Except some pioneering studies in Hymenopterans (7)(8)(9)(10)(11) and Lepidopterans (12), little is known about how these different PNs connect in the olfactory circuit and work physiologically. As the most studied PN type in Drosophila, the cholinergic PNs (mPNs) form the medial antennocerebral tract and convey excitatory signals encoding odor identity and intensity (13)(14)(15) that are necessary for the fly to perform appropriate behaviors (16,17).…”

Insect chemoreception: a tribute to John G. Hildebrand

“…The importance of temporal aspects in coding behaviorally relevant odorant mixtures is demonstrated by Martin et al (2013) using multi-unit electrophysiological recordings of AL neurons and behaviorally relevant mixtures of sex-pheromone components in Manudca sexta. The contribution by Rössler and Brill (2013) focuses on neurophysiological, anatomical and evolutionary aspects of parallel processing of olfactory information along the olfactory pathway, in particular using simultaneous multi-unit recordings from two sets of AL projection neurons within a dual olfactory pathway in the honeybee . The contribution by Lei et al (2013) concludes this section by presenting new results on processing of sex-pheromone information by protocerebral neurons in Manduca sexta.…”