The primacy model and the structure of olfactory space

Understanding sensory processing involves relating the stimulus space, its neural representation, and perceptual quality. In olfaction, the difficulty in establishing these links lies partly in the complexity of the underlying odor input space and perceptual responses. Based on the recently proposed primacy model for concentration invariant odor identity representation and a few assumptions, we have developed a theoretical framework for mapping the odor input space to the response properties of olfactory receptors. We analyze a geometrical structure containing odor representations in a multidimensional space of receptor affinities and describe its low-dimensional implementation, the primacy hull. We propose the implications of the primacy hull for the structure of feedforward connectivity in early olfactory networks. We test the predictions of our theory by comparing the existing receptor-ligand affinity and connectivity data obtained in the fruit fly olfactory system. We find that the Kenyon cells of the insect mushroom body integrate inputs from the high-affinity (primacy) sets of olfactory receptors in agreement with the primacy theory.Author summary: Sensory systems face the problem of computing stimulus identity that is invariant with respect to multiple stimulus features. In the olfactory system, odorant percepts often retain their identity despite substantial variations in the odorant concentration. How can olfactory networks robustly represent odorant identity despite variable stimulus intensity? In the nose, odorants are sensed by the odorant receptors (ORs), the specialized proteins that can be activated by the odorant molecules. In this study, we develop a theory for encoding concentration-invariant odor objects. We propose that the identities of a small group of the most sensitive ORs represent odorant identity in a concentration-invariant manner. We argue that, although absolute values of olfactory receptor responses may depend on concentration, their ranking remains invariant, leading to invariance in the membership of the most sensitive (primary) group. We call this form of representation of concentration invariant odorant identity the primacy coding model. We investigate the mathematical principles underlying the primacy coding model and test its predictions using connectivity and neuronal activations data from the fruit fly olfactory system. We find that neurons in the fly olfactory system integrate inputs from the high-affinity (primacy) sets of ORs in agreement with the primacy theory.