Dual olfactory pathway in the honeybee, Apis mellifera

Abstract

The antennal lobes (ALs) are the primary olfactory centers in the insect brain. In the AL of the honeybee, olfactory glomeruli receive input via four antennal sensory tracts (T1-4). Axons of projection neurons (PNs) leave the AL via several antenno-cerebral tracts (ACTs). To assign the input-output connectivity of all glomeruli, we investigated the spatial relationship of the antennal tracts and two prominent AL output tracts (medial and lateral ACT) mainly formed by uniglomerular (u) PNs using fluorescent tracing, confocal microscopy, and 3D analyses. Furthermore, we investigated the projections of all ACTs in higher olfactory centers, the mushroom-bodies (MB) and lateral horn (LH). The results revealed a clear segregation of glomeruli into two AL hemispheres specifically supplied by PNs of the medial and lateral ACT. PNs of the lateral ACT innervate glomeruli in the ventral-rostral AL and primarily receive input from T1 (plus a few glomeruli from T2 and T3). PNs of the medial ACT innervate glomeruli in the dorsal-caudal hemisphere, and mainly receive input from T3 (plus a few glomeruli from T2 and T4). The PNs of the m- and l-ACT terminate in different areas of the MB calyx and LH and remain largely segregated. Tracing of three mediolateral (ml) ACTs mainly formed by multiglomerular PNs revealed terminals in distinct compartments of the LH and in three olfactory foci within the lateral protocerebrum. The results indicate that olfactory input in the honeybee is processed via two separate, mainly uPN pathways to the MB calyx and LH and several pathways to the lateral protocerebrum.

Queen mandibular pheromone: questions that remain to be resolved

“…Local antennal-lobe interneurons (LNs), for example, can spread information from one glomerulus to another, and projection (output) neurons (PNs) can convey information to higher brain centres from one, or more glomeruli. Consistent with these possibilities, LNs generally extend processes to many glomeruli within the AL (Fonta et al 1993;Linster et al 2005;Sun et al 1993) and PNs in the honey bee vary in the number of glomeruli they innervate (Abel et al 2001;Brandt et al 2005;Kirschner et al 2006;Müller et al 2002). Uniglomerular PNs (uPNs), which send projections into a single glomerulus could convey information specific to one pheromone component, whereas PNs projecting to multiple glomeruli (multiglomerular PNs, mPNs) might instead integrate information originating from multiple glomeruli.…”

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.…”

“…Especially in the honeybee it has been shown recently that LNs provide patchy lateral connectivity and that different subpopulations possess elemental and configural olfactory coding properties 13,14 . The AL was shown to be subdivided into a ventral and a dorsal hemi lobe giving rise to the medial and the lateral antennal lobe tract (m-and l-ALT; formerly termed m-and l-APT for medial-and lateral antennal lobe protocerebral tract [15][16][17] ). Here a new tract terminology introduced by a recent effort for a unified nomenclature of the insect brain will be used 18 .…”

“…Here a new tract terminology introduced by a recent effort for a unified nomenclature of the insect brain will be used 18 . 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.…”

The anatomical pathways for antennal sensory information in the central nervous system of the cricket, Gryllus bimaculatus

“…LH). Previously the projection patterns of AL-PNs have been investigated in a wide variety of insects (fly: Stocker et al, 1990;cockroach: Malun et al, 1993;moth: Homberg et al, 1988, Rø et al, 2007; honeybee: Kirschner et al, 2006;ant: Zube et al, 2008). As in the other species studied we found in the cricket that the IACT was more frequently and more intensely stained.…”