Spatial projections to the olfactory bulb of functionally distinct and randomly distributed primary neurons in salmonid fishes

Abstract

In fish, olfactory sensory neurons expressing specific odorant receptors are randomly distributed throughout the olfactory epithelium, and, yet, these subsets of olfactory neurons segregate as they enter the olfactory bulb and project to restricted regions. We investigated the functional significance of this projection pattern by recording electroencephalographic responses (EEGs) from the olfactory bulb, while simultaneously monitoring electro-olfactograms (EOGs) in response to two distinct odorant groups, amino acids (AA) and a bile acid, taurocholic acid (TCA), in Atlantic salmon ( Salmo salar) and rainbow trout ( Oncorhynchus mykiss). EEGs to AA and TCA distributed in two segregated regions, lateroposterior and mid olfactory bulb. When olfactory rosettes were subjected to partial lamellectomy (removal of the anterior, posterior, medial, or lateral half), both EOGs and EEGs to these odorants were uniformly reduced, and the degree of reduction was not dependent on the rosette region removed. These results indicate that the entire rosette contributes to the generation of EOGs, leading to transmission to the bulb. We conclude that in salmonid fishes olfactory neurons responsive to AA and TCA are randomly distributed throughout the olfactory epithelium, and yet project to spatially segregated regions and thereby generated signals are encoded independently in the bulb.