Order code in the olfactory system.

Abstract

The ability to recognize odor identity across a wide range of concentrations is essential for natural olfactory behaviors. However, how odor identity is represented in the early olfactory system remains an open question. One theory proposes that glomeruli in the olfactory bulb, along with their associated odorant receptors (ORs), are activated by odorants in a temporal order that conveys information about odor identity. This order code is relatively robust to concentration changes, as the rank order of glomerular activation by a given odorant remains similar across concentrations. Alternatively, the primacy coding theory suggests that odor identity is defined by the most sensitive ORs, those that respond first, collectively referred to as the primacy set. To test these theories, we measured glomerular responses to a large set of odorants in the mouse olfactory bulb using calcium imaging. We found that receptor affinities can be embedded in a low-dimensional space (D = 10) with minimal loss of information. Within this space, we identified two clusters of glomeruli with distinct tuning properties that form independent odor representations. These clusters may correspond to the two phylogenetic classes of ORs, as revealed by both their functional characteristics and anatomical locations. In the OR affinity space, odorants evoke orderly activation waves whose directions can be used to define odor identities in the order coding model. Finally, we compared the order code and primacy model in predicting odor identity both across concentrations and across animals. Despite containing less information overall, the primacy model performed comparably to the order code. We confirmed the primacy models prediction that each receptor tends to contribute to the primacy set of at least one odorant. Analysis of binary odor mixtures revealed that mixture responses lie along geodesic lines connecting their component odors. Together, these findings suggest that odor information in the olfactory bulb may be represented through two complementary coding strategies: the primacy and order codes.