Calcium imaging in the ant Camponotus fellah reveals a conserved odour-similarity space in insects and mammals

Université de Toulouse
BMC Neuroscience (Impact Factor: 2.67). 02/2010; 11(1):28. DOI: 10.1186/1471-2202-11-28
Source: PubMed


Olfactory systems create representations of the chemical world in the animal brain. Recordings of odour-evoked activity in the primary olfactory centres of vertebrates and insects have suggested similar rules for odour processing, in particular through spatial organization of chemical information in their functional units, the glomeruli. Similarity between odour representations can be extracted from across-glomerulus patterns in a wide range of species, from insects to vertebrates, but comparison of odour similarity in such diverse taxa has not been addressed. In the present study, we asked how 11 aliphatic odorants previously tested in honeybees and rats are represented in the antennal lobe of the ant Camponotus fellah, a social insect that relies on olfaction for food search and social communication.
Using calcium imaging of specifically-stained second-order neurons, we show that these odours induce specific activity patterns in the ant antennal lobe. Using multidimensional analysis, we show that clustering of odours is similar in ants, bees and rats. Moreover, odour similarity is highly correlated in all three species.
This suggests the existence of similar coding rules in the neural olfactory spaces of species among which evolutionary divergence happened hundreds of million years ago.

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    • "The sensilla also contain ORNs that responded to several odorants associated with plants and other sources (Figure S2). From previous reports regarding ants and honeybees, it is also evident that they can detect and discriminate both pheromonal and non-pheromonal odors (Brill et al., 2013; Dupuy et al., 2010; Nishikawa et al., 2012; Rö ssler and Zube, 2011; Zube and Rö ssler, 2008). The characterization of responses to several hydrocarbons provided an opportunity to study the differential detection of the low-volatility compounds by a subset of the ant olfactory system. "
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    • "In these studies, however, only species belonging to the same family [Nymphalidae (Carlsson et al., 2011; Ômura and Honda, 2009)], subfamily [Heliothinae (Rostelien et al., 2005; Stranden et al., 2003); Murinae (Johnson et al., 2009; Soucy et al., 2009)], or genus [Drosophila (de Bruyne et al., 2010; Stensmyr et al., 2003)] were investigated. Remarkable similarities in olfactory coding were also found across the ant Camponotus fellah, the bee Apis mellifera and the rat Rattus norvegicus, i.e. between species belonging to different families (ant versus bee), or even to different phyla (ant versus rat) (Dupuy et al., 2010). However, only a small set of straight-chain aliphatic compounds was tested. "
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    ABSTRACT: The aim of the present study was to determine what impact phylogeny and life history might have on the coding of odours in the brain. Using three species of hawk moths (Sphingidae) and two species of owlet moths (Noctuidae), we visualized neural activity patterns in the antennal lobe, the first olfactory neuropil in insects, evoked by a set of ecologically relevant plant volatiles. Our results suggest that even between the two phylogenetically distant moth families, basic olfactory coding features are similar. But we also found different coding strategies in the moths' antennal lobe; namely, more specific patterns for chemically similar odorants in the two noctuid species than in the three sphingid species tested. This difference demonstrates the impact of the phylogenetic distance between species from different families despite some parallel life history traits found in both families. Furthermore, pronounced differences in larval and adult diet among the sphingids did not translate into differences in the olfactory code; instead, the three species had almost identical coding patterns.
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    • "If we can extrapolate the rough one-to-one relationship of receptors to glomeruli in Drosophila [8], [11] we can assume that these butterflies have approximately 60 receptor types. The odour-evoked responses in the AL showed similarities to what has been observed in other animals [13], [14], [15], [16], [17], [34], [35]. Most of the odorants evoked unique, though overlapping, patterns of activated glomeruli. "
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