Olfactory receptor neuronal dendrites become mostly intra-sustentacularly enwrapped upon maturity

Abstract

The mammalian olfactory epithelium (OE) sustains persistent neurogenesis even in the adult. Sustentacular cells therein play both epithelial and neuroglial roles, although their relation with olfactory receptor neurons (ORNs) and their function in ORN maturation remain insufficiently understood. Sustentacular wrapping of ORN dendrites has been long known but always considered a minor presence, as opposed to the supposedly unwrapped majority of ORN dendrites at inter-sustentacular borderlines. Using immunofluorescence, confocal and immuno-electron microscopy, the current study examined cytoarchitectonic organization and maturation of ORN dendrites at the rat OE apical layer. Contrary to common belief, the observations here on tangential histological sections of the OE apical junctional belt layer showed on average 53.93% sustentacular cell-enwrapped, 18.46% partially wrapped (in the vertical grooves on the sides of sustentacular apices) and 27.61% unwrapped ORN dendrites (at the borderlines between sustentacular cells). The enwrapped dendrites were found within the confines of sustentacular apices but linked to the sides of the latter each by a mesentery (mesodendrite) of sustentacular plasma membranes and autotypic cell junctions. Up to six dendrites were seen in one sustentacular apical process. As marked by high and low immunoreactivity for class III beta-tubulin, respectively, immature and mature ORN dendrites accounted on average for 12.46 and 87.54% of the total ORN dendrites at the OE apical layer. By correlative analysis of the maturity level and wrapping status, most immature ORN dendrites were found unwrapped (immature unwrapped = 9.71% of the total dendrites), and practically no immature dendrites appeared enwrapped. In contrast, mature ORN dendrites comprised all the enwrapped (mature enwrapped = 53.93% of the total), most of the partially wrapped (mature partially wrapped = 15.71% of the total) and a portion of the unwrapped ORN dendrites (mature unwrapped = 17.9% of the total dendrites). Based on the current findings and previous data by other researchers, it is concluded that immature ORN dendrites emerge vertically from the OE apical surface between sustentacular cell apices. A large majority of the newly emerged dendrites then undergo sideways migration, sustentacular enwrapment and further maturation. Only a small minority of the newly emerged dendrites reach maturity and remain unwrapped. These divergent maturational courses imply structural or functional differences between the enwrapped and unwrapped mature ORN dendrites.