Distinct subsets of sensory olfactory neurons in mouse: Possible role in the formation of the mosaic olfactory projection

Abstract

The axons of the primary sensory olfactory neurons project from the olfactory neuroepithelium lining the nasal cavity, onto glomeruli covering the surface of the olfactory bulb. Neuroanatomical studies have shown previously that individual olfactory glomeruli are innervated by neurons that are dispersed widely within the nasal cavity. The aim of the present study was to test the hypothesis that phenotypically unique subsets of primary sensory olfactory neurons, scattered throughout the nasal cavity, project to a subset of glomeruli in specific olfactory bulb loci. Immunochemical and histochemical analyses in neonatal mice revealed that the plant lectin, Dolichos biflorus agglutinin, bound to a subset of mature primary sensory olfactory neurons which express the olfactory marker protein. This subset of neurons was principally located in the rostromedial and dorsal portions of the nasal cavity and projected specifically to a subset of glomeruli in the rostromedial and caudodorsal portions of the olfactory bulb. Analysis of Dolichos biflorus-reactive axons revealed that these axons coursed randomly, with no evidence of their selective fasciculation, within the olfactory nerve. It was only at the level of the rostral olfactory bulb that a significant reorganisation of their trajectory was observed. Within the outer fibre layer of the bulb, discrete bundles of lectin-reactive axons began to coalesce selectively into fascicles which preferentially oriented toward the medial side of the olfactory bulb. These data demonstrated that a phenotypically distinct subset of primary sensory olfactory neurons exhibits a topographical projection from the olfactory epithelium to the olfactory bulb, and suggests that these, and other subsets, may form the basis of the mosaic nature of this pathway. Moreover, it appears that the outer nerve fibre layer in the rostral olfactory bulb plays an important instructive role in the guidance and fasciculation of olfactory sensory axons.

Development of olfactory glomeruli: Temporal and spatial interactions between olfactory receptor axons and mitral cells in opossums and rats

“…Even in the developing olfactory system, odor stimulation results in the activation of discrete numbers of glomeruli, perhaps because subsets of olfactory receptor neurons, characterized by common histochemical properties (Key and Akeson, 1993;Carr et al, 1994) and odorant receptor molecules (Ressler et al, 1994;Vassar et al, 1994) project to specific glomeruli. Mitral cells with dendritic processes in these regions would experience spatially and/or temporally synchronous activity, perhaps reinforcing the pattern of synaptic connections within a glomerulus via Hebbian rules (Hebb, 1949;Constantine-Paton et al, 1990;Goodman and Shatz, 1993).…”

Errors in lamina growth of primary olfactory axons in the rat and mouse olfactory bulb

“…Thus, olfactory axons may target the appropriate glomerulus in a precise manner. However, there are several reports that some primary olfactory axons bypass the glomerular layer in the olfactory bulb and reach as deep as the ventricular layer of the olfactory bulb during embryogenesis (Monti-Graziadei et al, 1980;Santacana et al, 1992;Key and Akeson, 1993;Treloar et al, 1996). Histochemical staining with the plant lectin Dolichos biflorus-agglutinin (DBA) also revealed a number of primary olfactory axons that grow past their appropriate postsynaptic target in the glomerular layer of the postnatal olfactory bulb but are eventually lost because no olfactory axons reside deep to the glomerular layer in the adult olfactory bulb (Key and Akeson, 1993).…”

Charting Plasticity in the Regenerating Maps of the Mammalian Olfactory Bulb

“…Because broad regions of the MOE and OB express glycoproteins, these molecules are not likely to mediate the targeting of OSN axons to specific glomeruli. However, axons expressing the same glycoproteins appear to sort into bundles within the nerve layer (Key and Akeson 1993) and may be involved in the fasciculation of OSN axons that express a given OR. Cell surface adhesion molecules are a second group implicated in the broad organization of OSN to OB projections.…”