Differential distribution of olfactory receptor neurons in goldfish: structural and molecular correlates

The olfactory system of many terrestrial vertebrates comprises a main olfactory organ and a vomeronasal organ each containing a morphologically distinct type of olfactory receptor neuron (ORN). The two cell types also differ in the expression of G-proteins and odorant receptor molecules. Fish do not have a vomeronasal organ, and their olfactory neurons-three different morphological types-are contained in one epithelium. The olfactory organ of goldfish appears as a rosette, with the sensory epithelium lying along the proximal portion of each lamella, where it attaches to the midline raphe. Using immunocytochemistry, in situ hybridization, and electron microscopy, we tested whether a correlation exists between receptor cell morphology, distribution of cell type within the sensory epithelium, and expression of odorant receptors and G-proteins. A strong correlation exists between ORN morphology, type of odorant receptor and G-protein expressed and the distribution of sensory cells within the olfactory epithelium. The Buck and Axel type of odorant receptor and Galpha(olf) are expressed in tall ciliated ORNs distributed homogenously across the entire sensory epithelium. In contrast, microvillous ORNs expressing V2R-like receptors, and Galpha(o), Galpha(q), or Galpha(i-3), and crypt type ORNs expressing Galpha(o) and Galpha(q), are preferentially located along the dorsal margin of the epithelium and near the midline raphe. V2R- and OR-type receptor molecules do not colocalize in one cell, and only crypt-type ORNs express more than one G-protein.