Interactions between odorant functional group and hydrocarbon structure influence activity in glomerular response modules in the rat olfactory bulb

Olfactory sensory neurons expressing the same odorant receptor gene typically send convergent projections to a pair of glomeruli in each olfactory bulb, one glomerulus of which is located in the lateral aspect and one in the medial aspect (Ressler et al., 1994; Vassar et al., 1994; Mombaerts et al., 1996). Pure odorants evoke spatial patterns of activity in the olfactory bulb that involve corresponding lateral and medial pairs of glomerular clusters, which presumably reflects the activation of subsets of odorant receptors recognizing particular molecular features of each odorant (Johnson et al., 1998; 1999; 2002; 2004a,b; Johnson and Leon, 2000a,b). The molecular features that are most important for activity in particular regions of the glomerular layer can be deduced from differences in activity across carefully chosen series of odorants differing systematically in chemical structure (Leon and Johnson, 2003). When we used odorants sharing a straight-chained feature but differing in oxygen-containing functional groups, we found that each functional group was associated with activity in one or more pairs of anterior glomerular clusters, while all odorants overlapped in their stimulation of other, more posterior pairs of glomerular clusters (Johnson and Leon, 2000a). This finding suggested that the anterior glomeruli might be particularly sensitive to functional group, while the posterior glomeruli might be specific for the hydrocarbon structure of the odorants. Indeed, homologous series of straight-chained odorants differing in carbon number but possessing the same functional group stimulated the same anterior areas but displayed more differences in the posterior bulb (Johnson et al., 1999; 2004a). Carboxylic acid odorants differing more dramatically in hydrocarbon structure, including branched, double-bonded and cyclic structures, also overlapped in their activation of the acid-associated, anterior glomerular module, but yielded different posterior activation patterns (Johnson and Leon, 2000b). Although there is some evidence that responses associated with functional groups other than carboxylic acids overlap for odorants of greatly differing hydrocarbon structure (Johnson et al., 2002), there has been no systematic study of widely different structures involving these other functional groups. Nor has there been a study to determine if there are glomeruli associated with particular hydrocarbon structural features by varying both hydrocarbon structure and functional group systematically. In the present study, we have exposed rats to 22 different odorants combining five different functional groups with five different hydrocarbon structural features to test whether all functional group-associated glomerular modules respond independently of hydrocarbon structure. We also have searched for areas of the bulb activated in common by odorants sharing particular hydrocarbon structures. In the course of this work, we found evidence that a unique region in the dorsal part of the bulb responded both to the ketone functional group and to aromatic structural features, which led us to study other aromatic odorants to explore the specificity of that module in greater detail.