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

Abstract

In an effort to understand mammalian olfactory processing, we have been describing the responses to systematically different odorants in the glomerular layer of the main olfactory bulb of rats. To understand the processing of pure hydrocarbon structures in this system, we used the [ 14 C]2-deoxyglucose method to determine glomerular responses to a homologous series of alkanes (from six to sixteen carbons) that are straight-chained hydrocarbons without functional groups. We found two rostral regions of activity evoked by these odorants, one lateral and one medial, that were observed to shift ventrally with increasing alkane carbon chain length. Furthermore, we successfully predicted that the longest alkanes with carbon chain length greater than our previous odorant selections would stimulate extremely ventral glomerular regions where no activation had been observed with the hundreds of odorants that we had previously studied. Overlaps in response profiles were observed in the patterns evoked by alkanes and by other aliphatic odorants of corresponding carbon chain length despite possessing different oxygen-containing functional groups, which demonstrated that hydrocarbon chains could serve as molecular features in the combinatorial coding of odorant information. We found a close and predictable relationship among the molecular properties of odorants, their induced neural activity, and their perceptual similarities. Keywordsalkanes; chemotopic organization; combinatorial coding; odor similarity; glomeruli; deoxyglucose; habituation Studies by a number of laboratories using odorants that differ systematically in molecular structures continue to support a combinatorial model of olfactory processing initially proposed by Polak (1973), in which molecular features of an odorant are recognized and encoded by the system (Kauer and Cinelli, 1993; Korsching, 1997, 1998;Joerges et al., 1997;Johnson et al., 1998Johnson et al., , 1999Johnson et al., , 2002Johnson et al., , 2004Johnson et al., , 2005aMalnic et al., 1999;Rubin and Katz, 1999;Sachse et al., 1999; Johnson and Leon, 2000a, b;Uchida et al., 2000;Belluscio and Katz, 2001;Fuss and Korsching, 2001;Meister and Bonhoeffer, 2001;Igarashi and Mori, 2005). 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.Corresponding author: Sabrina L. Ho, Unive...

Chemotopic odorant coding in a mammalian olfactory system

“…The phenomenon is seen for both primary alcohols and secondary alcohols with the hydroxyl group in the 2-position . The hydrocarbon chain-related domains (light blue in Figure 4) also show chemotopic progressions for all effective stimuli including esters, acids, alcohols, aldehydes, and alkanes (Johnson et al, 1998;2004;Inaki et al, 2002;Igarashi and Mori, 2005;Ho et al, 2006a).…”

“…For example, habituation among members of a homologous series of aliphatic acids or alkanes was proportional to the degree of similarity in their 2DG activity patterns (Cleland et al, 2002;Ho et al, 2006a). Quantitative similarities between 2DG patterns evoked by octane and/or by eightcarbon branched alkanes or eight-carbon alkenes and alkynes also predicted the amount of cross-habituation between the odorant pairs (Ho et al, 2006b).…”

“…In many experiments characterizing these progressions, odorants are presented at fixed vapor phase concentrations (Johnson et al, 1998;2004) or across a range of concentrations (Meister and Bonhoeffer, 2001), although similar progressions can be found without controlling odorant concentration (Rubin and Katz, 1999;Uchida et al, 2000;Johnson and Leon, 2000b;Inaki et al, 2002;Igarishi and Mori, 2005;Ho et al, 2006a). The suggestion that chemotopic progressions arise as an artifact of different odorant concentrations across a series (Wilson and Mainen, 2006) is therefore unfounded.…”

“…Such clusters often have a different set of chemical determinants for their activation. For example, aliphatic odorants often activate both glomerular domains directly related to their functional groups and domains related to their hydrocarbon chains (Johnson et al, 1998;2004;Johnson and Leon, 2000a,b;Ho et al, 2006a). …”

Understanding smell—The olfactory stimulus problem

“…In mice and humans the dorsal part of the OB was implicated in innate responses to aversive odorants (Kobayakawa et al, 2007;Rolls et al, 2003). Several studies have found a relationship between differences in behavior and shifts in spatial patterns (Ho et al, 2006;Linster et al, 2002) and, even more, changing locations of glomeruli in mice can result in behavioral impairments, in spite of persistent physiological activations (Adam and Mizrahi, 2010). Similarly, in the AL of female moths, glomeruli in a sexually dimorphic region specialize in odorants that are related to oviposition (Kalberer et al, 2010;Reisenman et al, 2009).…”