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

Abstract

SUMMARYTeleost 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. Supplementary material available online at

Aversive cues fail to activate fos expression in the asymmetric olfactory-habenula pathway of zebrafish

“…Crypt cells are relatively sparse compared to other OSNs (Hansen and Finger, 2000; Schmachtenberg, 2006) and, in zebrafish, appear to be nearly homogenous in their expression of the olfactory receptor gene, ora4 (Oka et al, 2012). Ligands for the Ora4 receptor are unknown, although there is evidence in the trout that crypt cells are most sensitive to sexual pheromones (Vielma et al, 2008; Bazaes and Schmachtenberg, 2012). The restricted expression of lhx2a coupled with the fact that ~10% of OSNs are ora4 negative, suggests that crypt cells are a diverse population and that the Ob-Ha pathway may sense a distinct odorant cue.…”

“…However, it is also possible that subcomponents of complex odorants such as fish flakes or conspecific extract masked or antagonized an activating cue (e.g., specific amino acids). Purified amino acids and specific components of sexual pheromones have been shown to elicit responses in the crypt cells of other fish species (Vielma et al, 2008; Bazaes and Schmachtenberg, 2012). …”

Neural circuits mediating olfactory-driven behavior in fish

“…A large majority of crypt cells respond to only one category of odorants. Intracellular recordings and calcium imaging studies carried out on mackerel and juvenile trout showed that different subsets of crypt cells respond either to amino acids, bile acids, or reproductive pheromones (Schmachtenberg, 2006; Vielma et al, 2008; Bazaes and Schmachtenberg, 2012). However, in mature trout, the majority of crypt cells respond to reproductive pheromones of the opposite sex and not to the other categories, indicating a change in the response profile of crypt cells during life, depending on sexual maturity and sex of the fish (Bazaes and Schmachtenberg, 2012).…”

Mixed input to olfactory glomeruli from two subsets of ciliated sensory neurons does not seem to impede relay neuron specificity in the crucian carp

“…Interestingly, transgenic studies in zebrafish revealed that ciliated OSNs do not share glomeruli with microvillous OSNs (Sato et al, 2005(Sato et al, , 2007 and recently, chondroitins were shown to be potent alarm substances that activate a mediodorsal locus in the zebrafish olfactory bulb (Mathuru et al, 2012), which is also activated by sex pheromones (Friedrich and Korsching, 1998). The mediodorsal region is innervated by crypt neurons expressing one type of receptor (Ahuja et al, 2013), which was reported to be activated by multiple ligands (Bazaes and Schmachtenberg, 2012;Vielma et al, 2008). Therefore, it might be that H3NO-and TLC-sensitive neurons express the same type(s) of receptor, but differentiate with respect to function and subcellular machinery.…”