Three distinct morphological classes of receptors in fish olfactory organs

Three morphologically distinct classes of receptor-neurons are proposed: (1) type I ciliar cells, (2) microvillar cells and (3) type II ciliar cells. Retrograde transport of horseradish peroxidase by axons in the olfactory nerve to the olfactory organs of goldfish (Carassius auratus) and channel catfish (Ictalurus punctatus) provided evidence that these axon-bearing cells are present in the organs of both species. Goldfish olfactory organs were also studied with scanning electron microscopy, dissociated with papain for isolated cell preparations, and processed for ultrastructural localization of acid phosphatase activity. Type I ciliar cells are similar to ciliar olfactory receptors found in all vertebrate classes. Microvillar cells are present in the olfactory organs of most fishes and in the tetrapod vomeronasal organ. In goldfish and catfish, type I ciliar and microvillar cells are concentrated on the inner third of each lamella, nearest to the median raphe. Type II ciliar cells have often been described as respiratory-type or ciliated nonsensory cells. They are structurally similar to respiratory epithelial cells in the nasal cavities of tetrapods and have motile cilia that beat synchronously, indicative of their role in mediating fluid flow over the olfactory epithelium. In goldfish they occur singly and in aggregates throughout the organ. In catfish they are segregated from type I ciliar and microvillar cells on the outer two-thirds of each lamella. In goldfish and catfish they have axons that pass through the olfactory nerve to the olfactory bulb; hence, they are receptor-neurons as well as analogous to respiratory epithelium. In addition to the three receptor types described above, cells resembling receptors with rodlike distal processes were seen filled with horseradish peroxidase and observed with scanning and transmission electron microscopy. Cells of similar structure have been documented elsewhere, often called "rod cells," and sometimes considered a separate receptor type in fishes. In this study, a number of rodlike processes were found with their ciliar or microvillar components partially fused. High levels of acid phosphatase activity were localized to these processes, and examples were found that corresponded to each of the three receptor types. Olfactory receptor turnover is believed to persist through life. The evidence presented supports the hypothesis that fusion of their dendritic apical processes marks an early stage of receptor cell senescence.