Local and global chemotopic organization: General features of the glomerular representations of aliphatic odorants differing in carbon number

Abstract

To determine whether there is a general strategy used by the olfactory system to represent odorants differing in carbon chain length, rats were exposed to homologous series of straight-chained, saturated aliphatic aldehydes, ethyl esters, acetates, ketones, primary alcohols, and secondary alcohols (32 odorants total). Neural activity across the entire glomerular layer of the olfactory bulb was mapped quantitatively by measuring uptake of [14C]2-deoxyglucose evoked by each odorant. Uptake was observed both in dorsal glomerular modules previously associated with the particular odorant functional groups and in more ventral and posterior modules. Aldehyde-evoked activity patterns were dominated by ventral modules that included the area receiving projections from octanal-responsive sensory neurons expressing the I7 odorant receptor. The dorsal area that has been the focus of optical imaging studies of aldehyde responses contained only minor activity. For all functional groups except for ketones, uptake within functional group-sensitive modules displayed local chemotopy, with longer odorants stimulating more ventral and rostral glomeruli. In more posterior regions, chemotopy was observed for all functional groups, again with uptake shifting ventrally and rostrally with increasing chain length. In addition to these local shifts in activity, correlations analysis of entire activity patterns revealed a global chemotopic organization for all odorant series, with each odorant evoking a pattern most similar to odorants possessing the same functional group but differing by only one carbon in length. Thus, global chemotopy and local modular chemotopy appear to be fundamental principles underlying the representation of odorants differing in carbon chain length.

Activity-dependent gating of lateral inhibition in the mouse olfactory bulb

“…Functionally, this will increase the separation between those cells that are firing at the highest rates and those firing at intermediate or lower rates, resulting in a kind of contrast enhancement that does not depend on spatial features of the representation. Although results from our model indicate that input patterns are decorrelated in a manner that is independent of spatial patterning, this does not rule out a role for the broad groupings of olfactory receptor types that have been reported 39,40 . This broad grouping could function to ensure that mitral cells responding to related odors are located in regions that are linked by their lateral dendrites and associated granule cells.…”

Long hydrocarbon chains serve as unique molecular features recognized by ventral glomeruli of the rat olfactory bulb

“…According to this model, odorants that share a molecular feature should be recognized by the same type of olfactory receptors to produce overlapping neural activity. To test this prediction, and to understand how the olfactory system responds to various molecular features, our laboratory has been studying responses to hundreds of odorants in the glomerular layer of the rat main olfactory bulb (Johnson et al, 1998(Johnson et al, , 1999(Johnson et al, , 2002(Johnson et al, , 2004(Johnson et al, , 2005a Johnson and Leon, 2000a, b;Linster et al, 2001a). In an effort to understand the processing of pure hydrocarbon structures in this system, we determined in this study the response to a series of alkanes, which are straight-chained hydrocarbons without functional groups.…”

“…We therefore hypothesize that the previously unresponsive ventral area might respond to even larger odorants than we had yet studied (Johnson et al, 2002). Since straight-chained alkanes remain volatile even at great molecular length, we used the [ 14 C]2-deoxyglucose (2-DG) method developed by our laboratory to examine glomerular responses to a homologous series varying from six to sixteen carbons, and predicted that responses to the larger odorants in this series would be observed in the mid-ventral area of the bulb.Even though glomerular responses have been observed to be organized topographically and have been found to be correlated with a number of molecular features of odorous stimuli (Imamura et al, 1992;Katoh et al, 1993; Korsching, 1997, 1998;Joerges et al, 1997;Johnson et al, 1998Johnson et al, , 1999Johnson et al, , 2002Johnson et al, , 2004Johnson et al, , 2005a Johnson and Leon, 2000a, b;Fuss and Korsching, 2001;Meister and Bonhoeffer, 2001;Takahashi et al, 2004;Igarashi and Mori, 2005), it remains unclear whether such chemotopic information is maintained through downstream perceptual processing, so that odorant-evoked responses in the olfactory bulb would predict perceptual phenomena such as odor recognition and discrimination. Indeed, few studies have examined directly the relationship between the similarity of overall glomerular responses and perceived odor similarity (Linster et al, 2001a;Cleland et al, 2002).…”

“…The extreme ventral activation can be appreciated more readily when a pattern (circled in pink) evoked by the 15-carbon alkane, pentadecane, was overlaid onto a 3-dimensional glomerular layer model that has been rotated to show the response on the ventral midline of the bulb (Fig. 1).The chemotopic progression of glomerular responses was examined further with a centroid analysis (Johnson and Leon, 2000a, b;Johnson et al, 2004Johnson et al, , 2005a. The centroid of 2-DG uptake was calculated separately for the lateral and the medial aspects of individual matrices within the region outlined in black in Figure 1.…”

Functional units in the olfactory system

“…The axons of sensory neurons expressing the same odorant receptor converge into glomeruli, which are organized into modular clusters that respond differentially to aspects of shared odorant chemistry, such as functional groups, hydrocarbon structure, and͞or chemical properties, that are determined by the whole molecule (7). Glomerular modules in the ventral half of the bulb have responses organized such that larger molecules activate more ventral glomeruli, a pattern that probably reflects chromatographic separation of odorants in the epithelium (8).…”