The how, when, and what of odor valence communication between the olfactory bulb and piriform cortex

Abstract

A core function of the olfactory system is to determine an odor’s valence. The central processing of odor valence is initiated in the olfactory bulb, but the neural mechanisms by which this important information is communicated to, and from, the olfactory cortex (piriform cortex) in humans are not known. To assess communication between the two nodes, we simultaneously measured odor-dependent neural activity in the olfactory bulb and piriform cortex from human participants while obtaining trial-by-trial valence ratings. We determinedwhenvalence information was communicated,whatkind of information was transferred, andhowthe information was transferred (i.e., in which frequency band). Support vector machine learning on the coherence spectrum and frequency-resolved Granger causality were used to identify valence-dependent differences in functional and effective connectivity between the olfactory bulb and piriform cortex. We found that the olfactory bulb communicates odor valence to the piriform cortex in the gamma band shortly after odor onset, while the piriform cortex subsequently feeds valence-related information back to the olfactory bulb in the beta band. Decoding accuracy was better for negative than positive valence, suggesting negative valence superiority. Critically, we replicated these findings in an independent dataset using other odors across a larger perceived valence range. Combined, these results demonstrate that the olfactory bulb and piriform cortex communicate levels of odor pleasantness across multiple frequencies, at specific time-points and in a direction-dependent pattern in accordance with the two-stage model of odor processing. It also provides further evidence that odor valence should be viewed as two perceptual dimensions and not one continuous.