Effects of functional group position on spatial representations of aliphatic odorants in the rat olfactory bulb

Abstract

Principles of olfactory coding can be clarified by studying the olfactory bulb activity patterns that are evoked by odorants differing systematically in chemical structure. In the present study, we used series of aliphatic esters, ketones, and alcohols (27 odorants total) to determine the effects of functional group position on glomerular-layer activity patterns. These patterns were measured as uptake of [(14)C]2-deoxyglucose and were mapped into standardized data matrices for statistical comparison across different rats. The magnitude of the effect of position differed greatly for the different functional groups. For ketones, there was little or no effect of position on evoked patterns. For esters, uptake in individual glomerular modules increased, whereas uptake in others decreased with changing group position, yet the overall patterns remained similar. For alcohols, group position had a profound effect on evoked activity patterns. For example, moving the hydroxyl group in either heptanol or nonanol from the first to the fourth carbon changed the activity patterns so greatly that the major areas of response did not overlap. Within every functional group series, however, responses were globally chemotopic, such that pairs of odorants with the smallest difference in functional group position evoked the most similar patterns. These results help to define further the specificities of glomeruli within previously described glomerular modules, and they show that functional group position can be an important feature in encoding an odorant molecule.

Fig. 1

Color-coded contour charts illustrating patterns of glomerular layer 2-DG uptake evoked by alcohol odorants. These charts represent data matrices averaged across multiple rats and are presented as rolled-out maps of the glomerular layer as if a cut had been made dorsally running anterior to posterior. Anterior is located on the left and lateral is in the top half of the charts. The ventral surface is positioned horizontally at the center of each chart (see “orientation” panel). The amount of uptake in units of z scores is indicated using colors as shown in the key. The “modules” inset shows locations of glomerular modules derived from responses to 54 previously studied odorants (Johnson et al., 2002). Modules discussed in depth regarding the representations of the odorants are superimposed on the contour charts. Dorsal-centered and simulated 3-dimensional versions of the same patterns can be found on our website (http://leonlab.bio.uci.edu).

Fig. 2

Modular responses. Uptake of 2-DG across each module (see Figure 1) was averaged for each odorant-evoked z score pattern. Each modular value then was expressed as a fraction of the maximum modular value evoked by the same odorant in the same bulbar aspect (lateral or medial). These ratios were used to adjust the diameters of circles to represent the relative stimulation of each module. Only positive values are shown. Lateral modules are labeled with lower case letters and are symbolized using solid circles, while paired medial modules are labeled with the corresponding upper case letter and are symbolized by open circles. The similarity in the average activation of paired modules likely represents the paired lateral and medial projection of sensory neurons expressing the same odorant receptor gene (Vassar et al., 1999; Ressler et al., 1999). Because uptake is averaged across entire modules, small foci of elevated 2-DG uptake, such as those occurring in module “A” for ethyl butyrate, propyl propionate, methyl caproate, and ethyl valerate (see Figure 1) are diminished in impact or even obscured in this figure, which nevertheless captures and simplifies the principal differences in the representations of both different functional groups (e.g., esters versus ketones) and different isomers (e.g., 1-heptanol versus 4-heptanol or 1-nonanol versus 4-nonanol).

Fig. 3

Patchworks of correlation coefficients reveal global chemotopy with respect to functional group position for esters and alcohols. Each patchwork represents Pearson’s correlation coefficients obtained by correlating every pair of averaged data matrices within an odorant series. Individual isomers of heptanol (C7 alcohols) and nonanol (C9 alcohols) are identified by their substitution position. Individual esters are indicated by abbreviations: mc, methyl caproate; ev, ethyl valerate; pb, propyl butyrate; bp, butyl propionate; aa, amyl acetate. Global chemotopy is evident from the higher correlation coefficients for odorants substituted at adjacent positions (i.e., along the diagonal of the patchwork).

Fig. 4

Contour charts illustrating patterns of glomerular layer uptake evoked by ester odorants. The charts are oriented as in Figure 1. The boundaries of modules containing foci of 2-DG uptake that are discussed in greater detail in the text are superimposed on the charts.

Fig. 5

Modules “a”/“A” and “b”/“B” display different effects of ester group position on amounts of modular 2-DG uptake. Shown here are responses to isomers of seven-carbon esters differing in their alcohol portion from one carbon (methyl caproate) to five carbons (amyl acetate). For each rat, uptake across modules was averaged in units of nCi/g wet weight of tissue and was divided by the average uptake measured in the same units in the subependymal zone of a restricted range of coronal sections from the same rat (Johnson et al., 1999). Error bars denote the standard error of the mean across the different animals. Modules “a” and “A” show a progressive decrease in 2-DG uptake as the alcohol portion lengthens (and the acid portion shortens), while modules “b” and “B” show a U-shaped curve indicating greater uptake when the ester bond is on either side of the molecule.

Fig. 6

Contour charts illustrating patterns of glomerular layer uptake evoked by ketone odorants. The charts are oriented as in Figures 1 and 4. The boundaries of modules “c” and “C”, which encompass areas of 2-DG uptake previously associated with ketones, are superimposed on the charts.

Fig. 7

Positional isomers of ketones do not differ in the amount of 2-DG uptake evoked in modules “c” and “C”. Uptake of 2-DG was averaged over modules as described for Figure 5. Error bars denote the standard error of the mean across the different animals.