Target tissue influences the peripheral trajectory of mouse primary sensory olfactory axons

Abstract

Primary olfactory neurons situated in the nasal septum project axons within fascicles along a highly stereotypical trajectory en route to the olfactory bulb. The ventral fascicles make a distinct dorsovental turn at the rear of the septum so as to reach the olfactory bulb. In the present study we have used a brain and nasal septum coculture system to examine the role of target tissue on the peripheral trajectory of olfactory sensory axons. In cultures of isolated embryonic nasal septa, olfactory axons form numerous parallel fascicles that project caudally in the submucosa, as they do in vivo. The ventral axon fascicles in the septum, however, often fail to turn, and do not project dorsally towards the roof of the nasal cavity. The presence of olfactory bulb, cortical, or tectal tissue apposed to the caudal end of the septum rescued this phenotype, causing the ventral fascicles to follow a normal in vivo-like trajectory. Ectopic placements of the explants revealed that brain tissue is not tropic for olfactory axons but appears to maintain the peripheral trajectory of growing axons in the nasal septum. Although primary olfactory axons are able to penetrate into olfactory bulb in vitro, they only superficially enter cortical tissue, whereas they do not grow into tectal explants. The ability of axons to differentially grow into different brain regions was shown to be unrelated to the migratory behavior of olfactory ensheathing cells, indicating that olfactory axons are directly responsive to guidance cues in the brain.

Deletion of voltage‐gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system

“…In fact, convergence of P2 axons has been demonstrated to be completely independent of the presence of the OB (St. John et al, 2003), but the refinement of these synaptic connections once they have arrived at the OB is what is perturbed without Kv1.3. Implantation, organo-typic co-cultures, and organ ablation studies collectively support a dynamic development of the combined olfactory epithelium and the laminar organization of the olfactory bulb (Graziadei et al, 1978(Graziadei et al, , 1979Storan and Key, 2004;Chehrehasa et al, 2006). At the same time, each organ can develop independently in vivo or in vitro in the absence of normal pathfinding cues.…”

“…For example, OSNs can fasciculate or even regenerate following complete surgical bulbectomy or in mouse genetic models that lack the OB or lack interactions between the OB and OE, and they can also project into foreign target tissues (Graziadei et al, 1978;Long et al, 2003;St. John et al, 2003;Storan and Key, 2004). In contrast, peripheral genetic ablation of the MOE can cause the misorientation of mitral cell dendrites (López-Mascaraque et al, 2005).…”

β1,3-N-Acetylglucosaminyltransferase 1 Glycosylation Is Required for Axon Pathfinding by Olfactory Sensory Neurons

“…A plausible mechanism for such a function could involve galectins, a family of lactosamine-binding proteins, because several members of this family are expressed in the axon pathways (Mahanthappa et al, 1994;Storan and Key, 2004). In the olfactory system, galectin-1 is expressed by ensheathing glial cells in axon tracts between the OE and OB and is capable of modulating olfactory axon-axon interactions in vitro (Mahanthappa et al, 1994).…”

“…Cell-surface carbohydrates are an additional source of neuronal heterogeneity (Crandall et al, 2000;Lipscomb et al, 2002;Gibson et al, 2004;Storan and Key, 2004). The stereotyped distribution of glycan-expressing glomeruli has led to the hypothesis that glycans may directly influence targeting of sensory axons (Lipscomb et al, 2003).…”

Lactosamine differentially affects olfactory sensory neuron projections to the olfactory bulb

“…The unique pattern of glycosylation exhibited by olfactory projections has led to considerable interest in the function of carbohydrates in patterning connectivity between the OE and the OB (Crandall et al, 2000;Lipscomb et al, 2003;Gibson et al, 2004;Storan et al, 2004). We showed recently that one of these mosaically distributed glycans, the terminal disaccharide lactosamine, is required in mice for OB innervation by certain OSNs (Henion et al, 2005).…”