Configural and Elemental Coding of Natural Odor Mixture Components in the Human Brain

Abstract

SUMMARY Most real-world odors are complex mixtures of distinct molecular components. Olfactory systems can adopt different strategies to contend with this stimulus complexity. In elemental processing, odor perception is derived from the sum of its parts; in configural processing, the parts are integrated into unique perceptual wholes. Here we used gas-chromatography/mass-spectrometry techniques to deconstruct a complex natural food smell and assess whether olfactory salience is confined to the whole odor or is also embodied in its parts. By implementing an fMRI sensory-specific satiety paradigm, we identified reward-based changes in orbitofrontal cortex (OFC) for the whole odor and for a small subset of components. Moreover, component-specific changes in OFC-amygdala connectivity correlated with perceived value. Our findings imply that the human brain has direct access to the elemental content of a natural food odor, and highlight the dynamic capacity of the olfactory system to engage both object-level and component-level mechanisms to subserve behavior.

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“…Multivariate fMRI pattern analyses have shown that distributed ensemble representations in the PC exhibit greater pattern overlap for odor stimuli belonging to the same perceptual category [50]. A recent study demonstrated that the posterior PC encodes value-based ensemble codes of a complex natural food-odor (peanut butter), but not its chemical components [51], consistent with the idea of configural processing in this area. Non-olfactory cues may also elicit odorspecific distributed patterns in the posterior PC in advance of odor input [52,53], suggesting that this area receives top-down projections to facilitate olfactory predictive coding and rapid processing [29].…”

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