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. 2010 Aug 22;277(1693):2465-74.
doi: 10.1098/rspb.2010.0366. Epub 2010 Apr 7.

Spatial representation of alarm pheromone information in a secondary olfactory centre in the ant brain

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Spatial representation of alarm pheromone information in a secondary olfactory centre in the ant brain

Nobuhiro Yamagata et al. Proc Biol Sci. .

Abstract

Pheromones play major roles in intraspecific communication in many animals. Elaborated communication systems in eusocial insects provide excellent materials to study neural mechanisms for social pheromone processing. We previously reported that alarm pheromone information is processed in a specific cluster of glomeruli in the antennal lobe of the ant Camponotus obscuripes. However, representation of alarm pheromone information in a secondary olfactory centre is unknown in any animal. Olfactory information in the antennal lobe is transmitted to secondary olfactory centres, including the lateral horn, by projection neurons (PNs). In this study, we compared distributions of terminal boutons of alarm pheromone-sensitive and -insensitive PNs in the lateral horn of ants. Distributions of their dendrites largely overlapped, but there was a region where boutons of pheromone-sensitive PNs, but not those of pheromone-insensitive PNs, were significantly denser than in the rest of the lateral horn. Moreover, most of a major type of pheromone-sensitive efferent neurons from the lateral horn extended dendritic branches in this region, suggesting specialization of this region for alarm pheromone processing. This study is the first study to demonstrate the presence of specialized areas for the processing of a non-sexual, social pheromone in the secondary olfactory centre in any animal.

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Figures

Figure 1.
Figure 1.
Structure of the l ho of the ant brain. (a) A frontal section of a Bodian-stained ant brain at a depth of approximately 120 μm from the frontal (ventral) surface. a lob, antennal lobe; l ho, lateral horn; ca, calyces of the mushroom body. (b) A magnified image of the lateral protocerebrum (inset in (a)), including the l ho. Two round structures at the anterior part of the l ho (red arrowheads), which we call antero-lateral l ho (al l ho), are delineated by the antenno-cerebral tract (ACT) and the anterior superior optic tract (a.s.o.t). In addition, an ellipsoidal structure at the lateral edge of the l ho, lateral l ho (l l ho), is also visible. (c) Terminal arborizations of a class of uni-PN (type 1 uni-PN), the axon of which passes through the medial antenno-cerebral tract (m-ACT), seen as a confocal image at a depth of 70–140 µm from the frontal surface. Their terminal branches are located in the anterior part of the lateral l ho (region denoted by yellow broken line) and nearby l ho region (region denoted by black broken line). Grey broken line in (c), as well as in (d) and (h), depicts outline of the l ho at this depth. (d) Terminal arborizations of another class of uni-PN (type 2 uni-PN). This type terminates in the posterior part of the lateral l ho (yellow broken line) and nearby l ho region (black broken line). (e) A type 1 uni-PN with terminal arborizations (arrowheads) in the antero-lateral l ho (magenta broken lines). (f,g) A three-dimensional reconstruction of the lateral l ho, and the antero-lateral l ho, and nearby protocerebral neuropils, viewed (f) ventrally and (g) posteriorly. The antero-lateral l ho is positioned postero-laterally to the mb, and the lateral l ho is positioned postero-medially to the medulla (me) and lobula (lo). ped, pedunculus. (h) The axon of a multiglomerular PN (multi-PN) bifurcates (arrowhead and double arrowhead), each forming dendritic branches in the l ho and in the area called the lateral network (ln) (Kirschner et al. 2006; Zube et al. 2008). (i) A schematic diagram of termination areas of type 1 uni-PNs (green), type 2 uni-PNs (blue) and multi-PNs (red) in the l ho. (j) Three-dimensional reconstruction of the distribution of terminal boutons of a multi-PN in the l ho, viewed ventrally and posteriorly. Scale bars: (a) 100 μm; (bh, j) 50 μm.
Figure 2.
Figure 2.
Three-dimensional reconstructions of distributions of terminal boutons of (a) three pheromone-sensitive and (b) three pheromone-insensitive uni-PNs in the l ho, viewed ventrally and posteriorly. The antero-lateral l ho (magenta) and the lateral l ho (khaki) are reconstructed as landmarks. Distributions of terminal boutons of pheromone-sensitive and pheromone-insensitive PNs are largely overlapped, but a region posterior to the antero-lateral l ho (blue) receives boutons from all of the three pheromone-sensitive PNs but from only one of the three pheromone-insensitive PNs. Boutons in the pheromone focus are coloured red and those in the rest of the l ho are coloured black. The neuron was sensitive or insensitive to formic acid (f±), n-undecane (u±) and non-pheromonal environmental odours (np±) tested. inhi.: the response was inhibitory. AS: alarm pheromone-sensitive glomerulus (Yamagata et al. 2006). The number for each pheromone-sensitive uni-PN in (a) corresponds to that in the electronic supplementary material, table S1 (scale bar, 50 μm).
Figure 3.
Figure 3.
Three-dimensional reconstructions of distributions of terminal boutons of (a) pheromone-sensitive and (b) pheromone-insensitive multi-PNs in the l ho, viewed ventrally and posteriorly. All eight pheromone-sensitive multi-PNs have terminal boutons in a region in which terminal boutons of pheromone-sensitive uni-PNs are densely distributed (blue). This is in contrast to the fact that only four (shown in broken square) of 11 pheromone-insensitive multi-PNs have terminal boutons in this region. AS+ and AS− indicate that the neuron had dendrites in at least one of the AS glomeruli and that the neuron had no dendrites in any of the AS glomeruli, respectively. All eight pheromone-sensitive multi-PNs innervated the AS glomeruli. Seven out of 11 pheromone-insensitive multi-PNs had densities in the AS glomeruli. Pheromone insensitivity of these multi-PNs is probably because they receive only a very weak synaptic input from the AS glomeruli. Notice that multi-PNs have dendrites in more than 50 glomeruli, among which only a few are the AS glomeruli. The number for each pheromone-sensitive multi-PN in (a) corresponds to that in the electronic supplementary material, table S1. For abbreviations, see legend of figure 2.
Figure 4.
Figure 4.
Distributions of terminal boutons of PNs in the putative pheromone focus and the rest of the l ho. (a) The percentage of the number of boutons in the putative pheromone focus was significantly greater for pheromone-sensitive PNs (n = 11) than that for pheromone-insensitive PNs (n = 14; p = 0.005, t-test). (b) The bouton density in the putative pheromone focus (inside) was significantly higher than that in the rest of the l ho (outside) in the case of pheromone-sensitive PNs (left, p = 0.01, n = 11, paired t-test), but not in the case of pheromone-insensitive PNs (right, p = 0.68, n = 14, paired t-test). phe+, pheromone-sensitive PNs; phe−, pheromone-insensitive PNs. s.e.m. as error bars. n.s.: non-significant, *p < 0.05, **p < 0.01.

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