Odorant tuning of olfactory crypt cells from juvenile and adult rainbow trout

Teleost fish lack independent olfactory organs for odorant and pheromone detection. Instead, they have a single sensory epithelium with two populations of receptor neurons, ciliated and microvillous, that are conserved among vertebrates, and a unique receptor cell type named the olfactory crypt cell. Crypt cells were shown to be chemosensory neurons that project to specific areas in the olfactory bulb, but their odorant tuning and overall function remain unclear. Reproduction in fish is generally synchronized by sex pheromonal signaling between males and females, but the sensors responsible for pheromone detection remain unknown. In crucian carp, a seasonal variation in the population of olfactory crypt cells and their brain projections pathways, involved in reproduction, led to the hypothesis of a role as sex pheromone detectors. In the present study, morphology and localization of olfactory crypt cells were compared between juvenile and mature rainbow trout of both sexes, and calcium imaging was used to visualize responses of crypt cells from the three groups to common social and food-related odorants, sex hormones and conspecific tissue extracts. Crypt cells from mature trout were found to be larger than those of juvenile specimens, and preferentially localized to the apical surface of the olfactory epithelium. Although a fraction of crypt cells of all groups responded to common odorants such as amino acids and bile salts, cells from mature trout showed a characteristic preference for gonadal extracts and hormones from the opposite sex. These results support an involvement of olfactory crypt cells in reproduction-related olfactory signaling in fishes.