Predicting odorant quality perceptions from multidimensional scaling of olfactory bulb glomerular activity patterns.

Abstract

Odorants and their perceptions differ along multiple dimensions, requiring that a critical examination of any putative neural code directly access the multidimensional nature of the encoding process. Previous work has examined simple, systematic odorant differences that, regardless of coding strategy, would be expected to produce simple, systematic predictions in neural and behavioral responses. Using an odorant identification confusion matrix task that extracts precise quality relationships across odorants, we determined whether spatially specific glomerular activity patterns predict perceptual quality relationships for odorants that cannot easily be classified a priori along a single chemical dimension. Multidimensional scaling analysis of odorant pattern similarity measures derived from the comparison of [ 14 C]-2-deoxyglucose glomerular activity pattern data yielded a twodimensional odorant activity space that was highly significantly predictive of similarly obtained odorant perceptual spaces, uniformly across animals. These results strongly support the relevance of global spatial patterns in the olfactory bulb to the encoding of odor quality. Keywordsodorant quality perception; bulbar activity patterns; 2-deoxyglucose The first step in the encoding of an odorant appears to be mediated by the binding of odorant molecular features to odorant receptors on olfactory sensory neurons (OSNs) (Malnic et al., 1999). Odorants stimulate distinct patterns of activity in the olfactory epithelium (Moulton, 1976;Scott & Brierly, 1999;Youngentob et al., 1995) that accurately predict psychophysically determined odorant quality perception (Kent et al., , 2003. By virtue of the highly organized OSN projections to the bulb (Mombaerts, 1996), the information displayed by glomeruli is a reflection of the OSN responses (Johnson & Leon, 2000a,b;Johnson et al., 1998Johnson et al., , 1999Johnson et al., , 2002Johnson et al., , 2005aUchida et al., 2000). Therefore, it has been hypothesized that odorant quality is represented through patterns of glomerular activation that enhance the patterned information established in the differential activation of OSNs (Kent et al., 2003;Mori et al., 1999;Youngentob et al., 1995). Consistent with this view are functional imaging studies demonstrating odorant specific patterns of glomerular activity (Johnson & Leon, 2000a,b;Johnson et al., 1998Johnson et al., , 1999Johnson et al., , 2002Johnson et al., , 2005a Meister & Bonhoffer, 2001;Uchida et al., 2000;Xu et al., 2003). Also suggestive are behavioral observations demonstrating that bulbar patterns of [ 14 C]-2-deoxyglucose (2-DG) glomerular uptake predict the differential ability of rats to perceive two chemically similar stimuli as different in an olfactory habituation/ Linster et al., 2001], homologous series [Cleland et al., 2002;Ho et al., 2006a] or similar hydrocarbons [Ho et al., 2006b]).The above notwithstanding, the molecules, neural responses, and perceptions involved in olfaction are by their nature multidimensional. Indeed, o...

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“…Previous experiments by our group and others have provided evidence for a predictive relationship between OB neural activity and odor perception (Cleland et al 2007;Kay and Laurent 1999;Youngentob et al 2006). Recently, this predictive relationship has been further tested by manipulations affecting both bulbar network computations and odor perception, demonstrating that changes in bulbar computation are predictive of changes in perception.…”

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“…The system was used with a chamber through which a constant flow of air could pass. As such, odorant stimuli were presented and exhausted from the testing chamber with the same level of stimulus control that is standard in our rigorous psychophysical testing paradigms (e.g., Youngentob, Johnson, Leon, Sheehe, & Kent, 2006;Youngentob, Margolis, & Youngentob, 2001;Youngentob, Markert, Mozell, & Hornung, 1990;Youngentob, Schwob, Sheehe, & Youngentob, 1997). The testing chamber consisted of a Plexiglass cylinder with a conical input and output designed to permit rapid onset and cleanout of each stimulus.…”