Primacy coding facilitates effective odor discrimination when receptor sensitivities are tuned

Abstract The olfactory system faces the difficult task of identifying an enormous variety of odors independent of their intensity. Primacy coding, where the odor identity is encoded by the receptor types that respond earliest, is one possible representation that can facilitate this task. So far, it is unclear whether primacy coding facilitates typical olfactory tasks and what constraints it implies for the olfactory system. In this paper, we develop a simple model of primacy coding, which we simulate numerically and analyze using a statistical description. We show that the encoded information depends strongly on the number of receptor types included in the primacy representation, but only weakly on the size of the receptor repertoire. The representation is independent of the odor intensity and the transmitted information is useful to perform typical olfactory tasks, like detecting a target odor or discriminating similar mixtures, with close to experimentally measured performance. Interestingly, we find situations in which a smaller receptor repertoire is advantageous for identifying a target odor. The model also suggests that overly sensitive receptor types could dominate the entire response and make the whole array useless, which allows us to predict how receptor arrays need to adapt to stay useful during environmental changes. By quantifying the information transmitted using primacy coding, we can thus connect microscopic characteristics of the olfactory system to its overall performance. Author summary Humans can identify odors independent of their intensity. Experimental data suggest that this is accomplished by representing the odor identity by the earliest responding receptor types. Using theoretical modeling, we here show that such a primacy code allows discriminating odors with close to experimentally measured performance. This performance depends strongly on the number of receptors considered in the primacy code, but the receptor repertoire size is less important. The model also suggests a strong evolutionary pressure on the receptor sensitivities, which could explain observed receptor copy number adaptations. Taken together, the model connects detailed molecular measurements to large-scale psycho-physical measurements, which will contribute to our understanding of the olfactory system.